Polarized Skylight Navigation in Insects: Model and Electrophysiology of e-Vector Coding by Neurons in the Central Complex

Abstract

Many insects exploit skylight polarization for visual compass orientation or course control. As found in crickets, the peripheral visual system (optic lobe) contains three types of polarization-sensitive neurons (POL neurons), which are tuned to different ( approximately 60 degrees diverging) e-vector orientations. Thus each e-vector orientation elicits a specific combination of activities among the POL neurons coding any e-vector orientation by just three neural signals. In this study, we hypothesize that in the presumed orientation center of the brain (central complex) e-vector orientation is population-coded by a set of "compass neurons." Using computer modeling, we present a neural network model transforming the signal triplet provided by the POL neurons to compass neuron activities coding e-vector orientation by a population code. Using intracellular electrophysiology and cell marking, we present evidence that neurons with the response profile of the presumed compass neurons do indeed exist in the insect brain: each of these compass neuron-like (CNL) cells is activated by a specific e-vector orientation only and otherwise remains silent. Morphologically, CNL cells are tangential neurons extending from the lateral accessory lobe to the lower division of the central body. Surpassing the modeled compass neurons in performance, CNL cells are insensitive to the degree of polarization of the stimulus between 99% and at least down to 18% polarization and thus largely disregard variations of skylight polarization due to changing solar elevations or atmospheric conditions. This suggests that the polarization vision system includes a gain control circuit keeping the output activity at a constant level.